Exploring a Novel Substrate‐Borne Vibratory Signal in the Wolf Spider Schizocosa Floridana

Received: 3 April 2020 | Revised: 23 October 2020 | Accepted: 1 November 2020 DOI: 10.1111/eth.13114 RESEARCH ARTICLE Exploring a novel substrate-borne vibratory signal in the wolf spider Schizocosa floridana Malcolm F. Rosenthal1 | Eileen A. Hebets2 | Rowan McGinley2 | Cody Raiza1 | James Starrett3 | Lin Yan1 | Damian O. Elias1 1University of California, Berkeley, CA, USA Abstract 2University of Nebraska – Lincoln, Lincoln, NE, USA Animals communicate using a diversity of signals produced by a wide array of physi- 3University of California, Davis, CA, USA cal structures. Determining how a signal is produced provides key insights into sig- Correspondence nal evolution. Here, we examine a complex vibratory mating display produced by Malcolm F. Rosenthal, University of male Schizocosa floridana wolf spiders. This display contains three discrete substrate- California, Berkeley, CA, USA. Email: [email protected] borne acoustic components (known as “thumps”, “taps”, and “chirps”), each of which is anecdotally associated with the movement of a different body part (the pedipalps, Funding information Division of Environmental Biology, Grant/ legs, and abdomen respectively). In order to determine the method of production, Award Number: 1940481; Division of we employ a combination of high-speed video/audio recordings and SEM imaging of Integrative Organismal Systems, Grant/ Award Number: 1556153 and 1556421 possible sound-producing structures. Previous work has suggested that the “chirp” component is tonal, a signal trait that would be potentially unique in the genus. We Editor: Marie Elisabeth Herberstein measured signal tonality for all courtship components, as well as for courtship components from sixteen other Schizocosa wolf spiders. Our results suggest that S. floridana produces courtship song using a combination of shared (palpal stridulation and foreleg percussion) and novel (abdominal movement) sound production mechanisms. Of particular interest, the “chirp”, which is produced using a novel abdominal production mechanism, is the only known tonal signal with acoustic properties that are unique within the genus. We argue that the potential evolution of a novel sound production mechanism has opened up a new axis of signaling trait space in this species, with important implications for how this signal is likely to function and evolve. KEYWORDS communication, spider, vibratory Hebets & Papaj, 2005; Pfennig & Pfennig, 2012), less work has fo- 1 | INTRODUCTION cused on how the physical mechanisms that produce these signals might drive their evolution (but see Elias et al., 2006). Understanding Animals produce a wide array of signals intended to modify the be- the physical mechanisms of signal production is critical, however, havior of other individuals to their benefit. The forms of these sig- as the nature of these mechanisms can both constrain and direct nals, which may be used to communicate in contexts ranging from signal evolution (e.g., Derryberry et al., 2012; Montealegre-Z, 2009; mate choice to predator avoidance, are famously diverse. Often, Podos, 2001). this variation is extensive even between closely related species. Specifically, whether new signals arise through new production Yet, while the roles of signaler, receiver, and environment in driving mechanisms or through modifications of pre-existing mechanisms is the divergence and evolution of new animal signals have received of particular interest, as this distinction dictates the constraints and considerable attention (e.g., Endler, 1992; Endler & Basolo, 1998; limitations under which these signals may evolve. Many, perhaps most, Ethology. 2020;00:1–10. wileyonlinelibrary.com/journal/eth © 2020 Wiley-VCH GmbH | 1 2 | ROSENTHAL et al. of the most commonly studied acoustic signals have arisen through the However, they cannot vary significantly in pitch, or perceived fre- modification of existing signal-producing structures (e.g., Ewing, 1989; quency. Tonal signals thus have the potential to vary along three in- Fitch, 2006). For example, the great diversity of birdsong derives from dependent axes (amplitude, temporal patterning, and pitch) whereas modifications in the use and form of a shared mechanism: the syrinx broadband signals vary along only two. Tonal variation can provide (Catchpole & Slater, 1995; Kingsley et al., 2018; Read & Weary, 1992; information to receivers. For example, pitch differences between Searcy & Andersson, 1986). And because the physical structure of individuals commonly reflect differences in body size (e.g., Gingras the avian vocal tract attenuates harmonic overtones, many bird songs et al., 2012; Hauser, 1993). Likewise, variations in pitch within in- share a similar pure-tone musical sound (Nowicki & Marler, 1988). dividuals can indicate signaler quality (Christie et al., 2004). Tonal These similarities are also potentially evidence of constraints, and the signals can also respond differently to changes in the environment. shared physical bases of the syrinx and of its associated neuromuscu- For example, narrow-bandwidth signals may respond differently to lar structures limit the trait space through which many bird songs are noise than other signals (Raboin & Elias, 2019) and may take advan- able to evolve (Podos et al., 2004). Likewise, for complex signals con- tage of unique spectral transmission properties of their environment taining multiple components, variation between signal components (e.g., McNett & Cocroft, 2008). A truly tonal chirp would thus open produced by the same structure might be limited (e.g., Reichert, 2013), up the possibility of S. floridana song varying in an axis that is known constrained by shared neuromuscular architecture (Arnold, 1992). to be important in many non-spider species, and that is not available Alternatively, novel signals, or signal components, produced by differ- to its congeners. ent production mechanisms may be more able to vary independently. In this study, we explore the spectral properties of the three Arthropod systems are well suited to the study of acoustic sig- major sounds produced by S. floridana. In particular, we focus on nal evolution (including both air- and substrate-borne acoustics; measurements of tonality, as pure-tone signals are unknown in this Ewing, 1989; Hill, 2008). Arthropods produce sound using a number of genus. To establish the presumptive acoustic novelty of the chirp, unique structures (Ewing, 1989; Uhl & Elias, 2011; Virant-Doberlet & we also compare its tonality with measurements made on court- Čokl, 2004), and their rigid exoskeleton means that new sound produc- ship signals from 16 of the 24 described North American species tion structures can evolve anywhere on the body (e.g., Jocqué, 2005; in the genus (Stratton, 2005). Additionally, we explore the poten- Virant-Doberlet & Čokl, 2004). Additionally, many arthropods produce tial mechanisms by which these courtship sounds are produced. complex vibratory songs that utilize the synchronous deployment of We use high-speed video recordings and SEM imaging of putative multiple distinct sound production mechanisms (Virant-Doberlet & sound-producing areas to begin assessing whether novelty in signal Čokl, 2004). We suggest that investigating how individuals produce acoustic properties is associated with modifications of pre-existing distinct signal components within a complex song, whether signal signal-producing mechanisms or the evolution of new structures/ components are produced using the same, different, new, or pre-ex- mechanisms. isting production mechanisms, and how members of one species differ from others in their sound production mechanisms are all key to understanding how complex signals evolve and function. 2 | METHODS Here, we investigate the acoustic properties and production mechanisms of the song of a common North American forest floor 2.1 | Animal collection and care arthropod—the wolf spider Schizocosa floridana (Bryant, 1934). Courting individuals in the wolf spider genus Schizocosa generate We collected immature S. floridana at night in Alachua County, substrate-borne songs to attract mates, with each species producing Florida, over two collection trips. Spiders used in courtship tonality a unique song. But though these songs are often distinguished in measurements and for scanning electron microscopy were collected their temporal patterning (see Hebets et al., 2013; Stratton, 2005), in February 2017. Spiders used in high-speed courtship recording the underlying production mechanisms are mostly common to wolf were collected in January 2019. In both cases, we transported spiders spiders in general (e.g., Hallander, 1967; Rovner, 1967). These mech- to UC Berkeley and individually housed them in 6 cm × 6 cm × 8 cm anisms include percussion of the pedipalps and the front pair of legs, clear plastic containers (Amac Plastic Products). The rearing room in and stridulation via specialized structures on the tibio-cymbial joint which they were housed was maintained on a 12 hr:12 hr light/dark of the pedipalp (Rovner, 1975). Schizocosa floridana song includes schedule at an ambient temperature of 25°C. We fed spiders one repeated production of three acoustic elements. Two of these (the body-size-matched cricket twice per week and provided them with “thump” and the “tap”) are broadband and atonal and are hypoth- ad libitum water. esized to be produced using stridulatory and percussive mechanisms common to the genus (Rosenthal & Hebets, 2012; Rundus et al., 2011). The third component,

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